Dissociation of automatic and strategic lexical-semantics: functional magnetic resonance imaging evidence for differing roles of multiple frontotemporal regions

Abstract

Behavioral research has demonstrated three major components of the lexical-semantic processing system: automatic activation of semantic representations, strategic retrieval of semantic representations, and inhibition of competitors. However, these component processes are inherently conflated in explicit lexical-semantic decision tasks typically used in functional magnetic resonance imaging (fMRI) research. Here, we combine the logic of behavioral priming studies and the neurophysiological phenomenon of fMRI priming to dissociate the neural bases of automatic and strategic lexical-semantic processes across a series of three studies. A single lexical decision task was used in all studies, with stimulus onset asynchrony or linguistic relationship between prime and target being manipulated. Study 1 demonstrated automatic semantic priming in the left mid-fusiform gyrus (mid-FFG) and strategic semantic priming in five regions: left middle temporal gyrus (MTG), bilateral anterior cingulate, anterior left inferior prefrontal cortex (aLIPC), and posterior LIPC (pLIPC). These priming effects were explored in more detail in two subsequent studies. Study 2 replicated the automatic priming effect in mid-FFG and demonstrated that automatic priming in this region is preferential for the semantic domain. Study 3 demonstrated a neural dissociation in regions contributing to the strategic semantic priming effect. Strategic semantic facilitation was observed in the aLIPC and MTG, whereas strategic semantic inhibition was observed in the pLIPC and anterior cingulate. These studies provide reproducible evidence for a neural dissociation between three well established components of the lexical-semantic processing system.

Figure 1.

Study 1 priming paradigm. The trial length was 2500 ms. The sequence of events was identical across short and long SOA trial types, differing only in timing. The prime was present for 250 ms during short trials (S) and 1000 ms during long trials (L). Primes were followed by a related (Rel), unrelated (Unrel), or pseudoword (Pseudo) target. Targets were followed by an ITI consisting of a series of letters, warning participants of the next trial.

Figure 2.

Study 2 priming paradigm. The trial length was 2000 ms. The prime was present for 150 ms and was followed by a semantically related (Sem), orthographically related (Orth), unrelated (Unrel), or pseudoword (Pseudo) target. Targets were followed by an ITI consisting of visual fixation (+).

Figure 3.

Study 3 priming paradigm. The trial length was 2500 ms. The prime was present for 1000 ms and was followed by a related (Rel), unrelated (Unrel), neutral (Nt), or pseudoword (Pseudo) target. Targets were followed by an ITI consisting of visual fixation (+).

Figure 4.

Study 1 RTs and priming effects. A, Mean RTs in milliseconds to targets preceded by related and unrelated primes, under short and long SOA conditions. B, Priming effects (unrelated − related) for short and long SOA conditions. ***p < 0.001. Error bars represent SEM. Numbers within bar charts represent exact RTs and priming effects.

Figure 5.

Study 1 MR priming effects. A, Whole-brain maps comparing all word conditions with visual fixation. B, Maps displaying regions activated by word pairs (A) that also show an effect of SOA, priming, or priming by SOA interactions. C, Priming effects in one region showing priming across short and long SOA conditions (left MTG) and three regions showing priming by SOA interactions (aLIPC, pLIPC, and left mid-FFG). A representation of the location of each ROI is overlaid on a high-resolution image of a single subject in standardized space to promote identification on a traditional axial slice. Peak Talairach coordinates of ROIs are given under structural images. Bar charts display mean MR percentage signal change from fixation for the short-related (SR), short-unrelated (SU), long-related (LR), and long-unrelated (LU) conditions. Colored bar charts show MR priming effects (unrelated − related) for short (S) and long (L) SOA conditions. ∗∗p < 0.01; ∗∗∗p < 0.005. Error bars represent SEM. M-FFG, Mid-FFG.

Figure 6.

Study 2 RTs and priming effects. A, Mean RTs in milliseconds to targets preceded by semantic (Sem), orthographic (Orth), and unrelated (Unrel) primes. B, Priming effects (unrelated − related) for targets preceded by semantic and orthographic primes. ∗∗∗p < 0.001. Error bars represent SEM. Numbers within bar charts represent exact RTs and priming effects.

Figure 7.

Study 2 MR priming effects. A, Whole-brain maps comparing all word conditions with visual fixation. B, Maps displaying regions activated by word pairs (A) that also show consistent priming across semantic and orthographic conditions, greater semantic priming, or greater orthographic priming. C, Priming effects in two regions showing semantic priming (left mid-FFG and left MTG), one region showing orthographic priming (a posterior portion of the posterior FFG), and one region showing priming across both conditions (an anterior portion of the posterior FFG). Bar charts display mean MR percentage signal change from fixation for the semantic (Sem), orthographic (Orth), and unrelated (Unrel) conditions. Colored bar charts show MR priming effects for the semantic and orthographic conditions. ∗∗p < 0.01. Error bars represent SEM. M-FFG, Mid-FFG; P-FFG, posterior FFG.

Figure 8.

Study 3 RTs and priming effects. A, Mean RTs in milliseconds to targets preceded by semantic (Rel), neutral (Nt), and unrelated (Unrel) primes. B, Facilitation (Fac) and inhibition (Inh) priming effects. ∗p < 0.05; ∗∗∗p < 0.001. Error bars represent SEM. Numbers within bar charts represent exact RTs and priming effects.

Figure 9.

Study 3 MR priming effects. A, Whole-brain maps comparing all word conditions with visual fixation. B, Maps displaying regions activated by word pairs (A) that also show an effect of facilitation (neutral > related) or inhibition (unrelated > neutral). C, Priming effects in two regions showing strategic semantic facilitation (aLIPC and left MTG) and two regions showing strategic semantic inhibition (pLIPC and left anterior cingulate gyrus). Bar charts display mean MR percentage signal change from fixation for the related (Rel), neutral (Nt), and unrelated (Unrel) conditions. Colored bar charts show MR priming effects of facilitation (Fac) and inhibition (Inh). ∗∗p < 0.01. Error bars represent SEM. ACG, Anterior cingulate gyrus.